An ecological analysis of stink bug and lepidopteran borer
complexes associated with pecan and citrus orchards in
the Vaalharts region
by
ANDRÉ VAN ROOYEN
Submitted in partial fulfilment of the requirements for the degree
MAGISTER SCIENTEAE IN ENTOMOLOGY
in the
Faculty of Natural and Agricultural Sciences
Department of Zoology & Entomology
University of the Free State
Bloemfontein, South Africa
SUPERVISOR: DR V.R. SWART
CO-SUPERVISOR: DR S.D. MOORE
i
DECLARATION
I, André van Rooyen, declare that the thesis hereby submitted by me for the Master of Science degree in Entomology at the University of the Free State is my own independent work and has not previously been submitted by me at another university/faculty. I furthermore concede copyright of the dissertation to the University of the Free State.
……….. ………..
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SUMMARY
This study investigates the insect-plant interactions on citrus fruit and pecan nuts in South Africa. The aims of this study were to determine whether lepidopteran borer pests shuttled between adjacent citrus and pecan orchards, and to establish the cultivar preference of the most prevalent stink bug borer species in Vaalharts pecan orchards. Pheromone trap data indicated that there was a significant overlap between the populations of false codling moth (Thaumatotibia leucotreta) and carob moth (Ectomyelois ceratoniae) between adjacent citrus and pecan orchards. Both species of moth were found within the citrus and pecan orchards. Larval eclosions indicated that false codling moths shuttled between adjacent citrus and pecan orchards; however, the direction of the shuttling could not be established. An abundance of citrus fruit drew false codling moths from an adjacent pecan orchard, which increased infestation in the citrus orchard. No significant evidence of carob moth shuttling was found. Adult false codling moths were found to be active throughout the winter, albeit in decreased numbers. Adult carob moths were almost entirely absent during the winter months, although larvae were still present in pecan nuts and citrus fruit. Grey-brown stink bugs (Coenomorpha
nervosa) were found to be the most prevalent hemipteran pest on pecan trees in the Vaalharts
region. Coenomorpha nervosa demonstrated a significant preference for pecan trees of the Wichita cultivar. Adult and nymph grey-brown stink bugs preferred the Wichita cultivar to Choctaw, Barton, and Navaho cultivars. The investigation could not find C. nervosa exploiting other viable food sources close to pecan orchards; even potential host plants that were not dead or defoliated during winter. Overall, the study indicates that adjacent citrus and pecan orchards will accommodate shuttling of false codling moths between orchards. Furthermore, grey-brown stink bugs were found to be the dominant hemipteran pest on pecan trees the Vaalharts region. Grey-brown stink bugs prefer the Wichita cultivar and do not exploit food sources near pecan trees of the Wichita cultivar.
Key terms: Lepidopteran borer shuttling, species overlap, false codling moth, carob moth, grey-brown stink bug, host preference, Wichita cultivar, Thaumatotibia leucotreta,
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OPSOMMING
Hierdie studie het die insek-plant-interaksies op sitrusvrugte en pekanneute in Suid-Afrika ondersoek. Die hoofdoelwitte van hierdie studie was om te bepaal of lepidoptera-boorderpeste tussen aangrensende sitrus- en pekanboorde migreer; asook om die kultivarvoorkeur van die mees algemene stinkbesieboorderspesie in Vaalharts-pekanboorde te bevestig. Feromoonlokvaldata het daarop gedui dat ’n beduidende oorvleueling tussen die bevolkings van valskodlingmot (Thaumatotibia leucotreta) en karobmot (Ectomyelois ceratoniae) tussen aangrensende sitrus- en pekanboorde teenwoordig was. Albei motspesies is gevind in die sitrus- en pekanboorde. Die uitbroei data van larwes het aangedui dat valskodlingmotte tussen aangrensende sitrus- en pekanboorde migreer. Die rigting van die migrasie kon egter nie vasgestel word nie. Oortollige hoeveelhede sitrusvrugte lok valskodlingmotte van ’n aangrensende pekanboord, wat lei tot verhoogde besmetting in die sitrusboord. Geen beduidende bewyse van karobmotmigrasie na aangrensende boorde kon gevind word nie. Daar is gevind dat valskodlingmotvolwassenes aktief is in die winter, maar in verminderde getalle. Karobmotvolwassenes was byna heeltemal afwesig gedurende die wintermaande, alhoewel larwes in beide pekanneute en sitrusvrugte teenwoordig was. Grys-bruin stinkbesies (Coenomorpha nervosa) was die mees algemene besieplaag op pekanbome in die Vaalhartsstreek. ’n Beduidende voorkeur vir pekanbome van die Wichita-kultivar is deur C.
nervosa gedemonstreer. Beide volwasse en nimf grys-bruin stinkbesies verkies die
Wichita-kultivar bo Choctaw-, Barton-, en Navaho-Wichita-kultivars. Dit kon nie bewys word dat C. nervosa voedselbronne naby pekanboorde gebruik nie, selfs potensiële gasheerplante wat nie in die winter ontbos of vrek nie. Die studie het getoon dat aangrensende sitrus- en pekanboorde migrasie van valskodlingmotte tussen boorde sal akkommodeer. Voorts is gevind dat grys-bruin stinkbesies die dominante besieplaag op pekanbome in die Vaalhartsstreek is. Grys-grys-bruin stinkbesies toon ’n voorkeur vir die Wichita-kultivar en maak nie gebruik van voedselbronne naby pekanbome van die Wichita-kultivar nie.
Sleutelterme: Lepidoptera boordermigrasie, spesiesoorvleueling, valskodlingmot, karobmot, pekan, sitrus, grys-bruin stinkbesie, gasheervoorkeur, Wichita-kultivar, Thaumatotibia
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ACKNOWLEDGMENTS
I would like to acknowledge the following people:
Dr Vaughn Swart; for his help and guidance with the project, arrangement of funding, and personal assistance on fieldwork excursions.
Dr Sean Moore; for his help and guidance with the project, the provision of delta traps, Lorlei pheromone ampules, and larval growth media.
Prof. Robert Schall; for the statistical analysis of the results and consultation regarding the data.
Mr Jaco Saaiman; for his assistance and companionship during monthly fieldwork excursions, and his friendship during the course of the study.
Ms Marguerite Westcott; for the identification of plant species for the alternate host study of C. nervosa.
Ms Liese Kilian for her support, encouragement and assistance during the final part of the thesis.
Mr Gerhard Booysen; for the provision of Pherolure packages.
Dr Martin Krüger; for the identification of false codling moth and carob moth specimens.
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TABLE OF CONTENTS
DECLARATION... i
SUMMARY... ii
OPSOMMING... iii
ACKNOWLEDGMENTS... iv
LIST OF FIGURES... ix
LIST OF TABLES
... xii
LIST OF ABBREVIATIONS
... xiii
CHAPTER 1: INTRODUCTION 1.1 Introduction ... 1
1.2 Ecology of false codling moth ... 2
1.2.1 History and taxonomy of false codling moth ... 2
1.2.2 Biology of false codling moth ... 2
1.2.3 Lifecycle of false codling moth... 5
1.2.4 Hosts of false codling moth ... 5
1.2.5 Geographical distribution of false codling moth ... 8
1.2.6 Control measures for false codling moth ... 9
1.3 Ecology of the carob moth ... 13
1.3.1 History and taxonomy of the carob moth ... 13
1.3.2 Biology of the carob moth ... 13
1.3.3 Lifecycle of the carob moth ... 15
1.3.4 Hosts of the carob moth ... 15
vi
1.3.6 Control measures of carob moth ... 18
1.4 Ecology of the grey-brown stink bug ... 22
1.4.1 History and taxonomy of the grey-brown stink bug ... 22
1.4.2 Biology of the grey-brown stink bug ... 22
1.4.3 Lifecycle of the grey-brown stink bug ... 23
1.4.4 Hosts of the grey-brown stink bug ... 24
1.4.5 Geographical distribution of the grey-brown stink bug ... 27
1.4.6 Control measures for grey-brown stink bug ... 27
1.5 References ... 31
CHAPTER 2: SHUTTLING OF FALSE CODLING MOTHS BETWEEN CITRUS AND PECAN ORCHARDS 2.1 Introduction ... 41
2.2 Materials and methods ... 42
2.3 Results ... 55 2.3.1 Combined captures ... 55 2.3.2 Seasonal fluctuation ... 62 2.3.3 Statistical analysis ... 62 2.4 Discussion ... 65 2.4.1 Species overlap ... 65 2.4.2 Shuttling ... 66
2.4.3 Pheromone trap predictability ... 66
2.4.4 Seasonal fluctuation ... 67
2.5 Conclusion ... 67
2.6 References ... 69
CHAPTER 3: SHUTTLING OF CAROB MOTHS BETWEEN CITRUS AND PECAN ORCHARDS 3.1 Introduction ... 71
vii
3.2 Materials and methods ... 73
3.3 Results ... 74 3.3.1 Combined captures ... 75 3.3.2 Seasonal fluctuation ... 80 3.3.3 Statistical analysis ... 81 3.4 Discussion ... 83 3.4.1 Species overlap ... 83 3.4.2 Shuttling ... 83
3.4.3 Pheromone trap predictability ... 84
3.4.4 Seasonal fluctuation ... 84
3.5 Conclusion ... 85
3.6 References ... 86
CHAPTER 4: PECAN CULTIVAR PREFERENCE AND THE EFFECT OF COVER CROPS AND NATURAL VEGETATION ON THE POPULATION OF THE GREY-BROWN STINK BUG 4.1 Introduction ... 89
4.2 Materials and methods ... 91
4.3 Results ... 100
4.3.1 Cultivar preference of C. nervosa ... 100
4.3.2 Possible alternative refuges for C. nervosa ... 100
4.4 Discussion ... 102
4.4.1 Cultivar preference ... 102
4.4.2 Alternate hosts for C. nervosa ... 102
4.5 Conclusion ... 103
4.6 References ... 104
CHAPTER 5: GENERAL CONCLUSIONS AND RECOMMENDATIONS 5.1 Introduction ... 106
viii
5.2 Discussion and recommendations ... 107
5.2.1 Infestation ... 107
5.2.2 Shuttling ... 108
5.2.3 Species overlap ... 109
5.2.4 Alternate host availability ... 109
5.2.5 Pheromone trap predictability ... 110
5.2.6 Pheromone specificity ... 110
5.2.7 Seasonal fluctuation ... 110
5.2.8 Cultivar preference of C. nervosa ... 111
5.2.9 Alternative host preference of C. nervosa... 112
5.3 General conclusion ... 112
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LIST OF FIGURES
Figure 2.1: Lepidopteran larvae and pupae within a cracked pecan nut. ... 44
Figure 2.2: An emergence box wherein pecan nuts were placed and moths were allowed to eclose. ... 44
Figure 2.3: Citrus fruit with a lepidopteran borer larva visible on the surface of the fruit. ... 45
Figure 2.4: Feeding canals and faecal matter were evident throughout the fruit. ... 45
Figure 2.5: Glass vials filled with the prepared growth medium wherein larvae collected from citrus fruit were allowed to mature, pupate, and eclose. Moths that emerged were found within the cotton wool. ... 46
Figure 2.6: Yellow delta trap suspended in a pecan tree (Carya illinoinensis); traps were generally placed where they were both easy to spot at a distance and easy to reach without the use of a ladder. ... 47
Figure 2.7: A sticky liner placed within the yellow delta traps. ... 47
Figure 2.8: Citrus control study site (located at S27°99'785", E24°75'174"). ... 48
Figure 2.9: Pecan control study site (located at S27°64'218", E24°74'293"). ... 49
Figure 2.10: Gillyfrost study site (located at S27°64'432", E24°77'325"). ... 50
Figure 2.11: Ouplaas study site (located at S27°66'702", E24°74'226"). ... 51
Figure 2.12: Floors Farm study site (located at S27°65'078", E24°75'950"). ... 52
Figure 2.13: Saamfarm A study site (located at S28°00'216", E24°75'846"). ... 53
Figure 2.14: Saamfarm C study site (located at S27°99'640", E24°73'903"). ... 54
Figure 2.15: Results from the Gillyfrost study site. ... 56
Figure 2.16: Results from the Floors Farm study site. ... 57
Figure 2.17: Results from the Ouplaas study site. ... 58
Figure 2.18: Results from the Saamfarm A study site. ... 59
x
Figure 2.20: Results from the control study sites. ... 61
Figure 2.21: Overview of FCM pheromone trap captures over the course of the study from all the sites, indicating year-round adult activity. ... 62
Figure 3.1: Sticky liner placed within the yellow delta traps, with dust build-up already visible in this example. The PheroLure™ pheromone lure is visible in the centre of the sticky trap, affixed directly onto it. ... 74
Figure 3.2: Results from the Gillyfrost study site. ... 75
Figure 3.3: Results from the Floors Farm study site. ... 76
Figure 3.4: Results from the Ouplaas study site. ... 77
Figure 3.5: Results from the Saamfarm A study site. ... 78
Figure 3.6: Results from the Saamfarm C study site. ... 79
Figure 3.7: Results from both the pecan and citrus control sites. ... 80
Figure 3.8: This combined graph offers an overview of CM pheromone trap captures, over the course of the study, from all the sites. This indicates a lack of activity during the winter months. ... 81
Figure 4.1: Coenomorpha nervosa on a pecan nut. Photo by J. Saaiman. ... 92
Figure 4.2: Example of a site where stink bug populations were determined and sweeps were done. ... 92
Figure 4.3: Example of a field of adjacent alfalfa. The pecan orchard is to the left of the field. ... 93
Figure 4.4: Layout of transects at the Oberholtzer study site (located at S27°66'332", E24°78'903"). ... 94
Figure 4.5: Layout of transects at the Engelbrecht study site (located at S27°64'137", E24°73'702"). ... 95
Figure 4.6: Layout of transects at the De Villiers study site (located at S27°71'754", E24°79'006"). ... 96
Figure 4.7: Layout of transects at the Duvenhage study site (located at S27°73'244", E24°77'508"). ... 97
xi
Figure 4.8: Layout of transects at the Human study site (located at S27°84'901", E24°81'423"). ... 98 Figure 4.9: Layout of transects at the Erasmus study site (located at S27°85'744",
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LIST OF TABLES
Table 2.1: Spearman correlation coefficients from pheromone trap captures for the Floors Farm study site. ... 63 Table 2.2: Spearman correlation coefficients from pheromone trap captures for the
Ouplaas study site. ... 63 Table 2.3: Spearman correlation coefficients of FCM reared from collected citrus fruit
and pecan nuts for the Floors Farm study site. ... 63 Table 2.4: Spearman correlation coefficients from the pheromone trap data for the Floors Farm study site. ... 64 Table 2.5: Spearman correlation coefficients for FCM reared from collected citrus fruits
and pecan nuts from the Ouplaas study site. ... 64 Table 2.6: Poisson regression of the FCM pheromone captures for the Floors Farm study
site. ... 65 Table 2.7: Poisson regression of the FCM pheromone captures for the Floors Farm study
site. ... 65 Table 3.1: Spearman correlation coefficients for CM reared from collected citrus fruit and
pecan nuts for the Gillyfrost study site. 82
Table 3.2: Spearman correlation coefficients for CM reared from collected citrus fruit and pecan nuts for the Floors Farm study site. ... 82 Table 3.3: Poisson regression of the CM pheromone captures for the Ouplaas study
site. ... 83 Table 4.1: Summary of the results for C. nervosa cultivar preference at all study
xiii
LIST OF ABBREVIATIONS
ARC Agricultural Research Council
BFAP Bureau for Food and Agricultural Policy
CM Carob moth
CRI Citrus Research International
DAFF Department of Agriculture, Forestry and Fisheries
EPPO European and Mediterranean Plant Protection Organization
EU European Union
FCM False codling moth
GENMOD General Linear Model Analysis IPM Integrated pest management SAS Statistical Analysis Software SIT Sterile insect technique UFS University of the Free State USA United States of America
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CHAPTER 1
INTRODUCTION
1.1 Introduction
The pecan nut and citrus industries in South Africa are important primary industries, with exports to the Northern Hemisphere offering significant capacities to absorb South African produce. Export markets to Africa, Asia, and the European Union (EU) all yielded positive trade deficits from 2013 onwards (Bureau for Food and Agricultural Policy (BFAP) 2015). Due to the isolated location and climate of South Africa, agricultural pests that are not historically native to the more temperate regions of the world could be introduced along with export products. Strict evidence-based phytosanitary measures that are the least trade restrictive possible should be employed, and should only be maintained with sufficient scientific evidence (Theyse 2010)
The false codling moth (FCM), Thaumatotibia leucotreta (Meyrick) [Lepidoptera: Tortricidae], is a registered phytosanitary pest for the United States of America (USA) and certain markets in the Far East. It is thus a concern to these export partners; primarily due to the polyphagous capabilities of the larvae and the difficulty of controlling the species with conventional pesticide treatment regimens (Department of Agriculture, Forestry and Fisheries (DAFF) 2016). The efficient and accurate identification of FCM larvae is also of concern. The carob moth (CM), Ectomyelois ceratoniae (Zeller) [Lepidoptera: Pyralidae] is an essentially cosmopolitan species that is visually distinct from FCM during the adult stage, which simplifies identification. Differentiation between FCM and CM larvae is more problematic and has the potential for confusion (Rentel et al. 2011). Similar larval feeding behaviours result in similar wounding patterns on infested fruit and similar physiological changes to the fruit. This causes potential complications; while it is not so much a threat to the export market as a whole, it might negatively affect individual shipments. It is therefore important to qualify the shuttling of these species between pecan nuts and citrus fruit. The effect of pecan orchards, planted proximally, must be quantified in the short term to ascertain if proximity increases infestation to a significant degree. In the longer term, this information can be used to make informed decisions regarding larger-scale integrated pest management (IPM) programmes.
2
If increased levels of infestation warrant such measures, farm and orchard layout might also need to be adjusted in order to mitigate the risk of the migrating moths.
The grey-brown stink bug, Coenomorpha nervosa Dallas (Hemiptera: Pentatomidae), is a pest of multiple crops in South Africa. In sufficient numbers, these hemipterans can cause substantial crop losses (Cissel et al. 2015). Even when larval feeding on the nuts is not sufficient to cause direct losses via nut drop or death, cosmetic damage to the kernel makes the nuts unmarketable. Even nuts sold for decorative purposes cannot be marketed if fed on by the grey-brown stink bug, as the nuts undergo physiological changes after the feeding which alter the external appearance of the nuts. It is thus important to know which cultivars are most at risk of being fed upon in order for measures to be taken to curtail losses for the valuable export market.
1.2 Ecology of false codling moth
1.2.1 History and taxonomy of false codling moth
Fuller described FCM in 1901; samples were discovered infesting citrus fruit in what is known as KwaZulu-Natal today (Schwartz 1981). Fuller named the moth “Natal codling moth” in 1901 and placed it in the genus of Carpocapsa. Howard referenced Enarmonia batrachopa in 1909 as the “orange codling moth”. In 1914, Kelly referred to E. batrachopa as the “false codling moth” which was found in acorns, also in what is today KwaZulu-Natal (Schwartz 1981). From then on, it was referred to as the false codling moth, or FCM. Meyrick, in 1913, described it as Argyroploce leucotreta, after which it was transferred to the genus
Cryptophlebia by Clarke in 1958, and thus renamed C. leucotreta (Newton 1998).
In 1999, Komai transferred the moth from genus Cryptophlebia to the previously synonymous genus of Thaumatotibia (Venette et al. 2003). False codling moth can be confused with species such as the codling moth (Cydia pomonella), macadamia nut borer (Thaumatotibia
batrachopa), and the litchi moth (Cryptophlebia peltastica) (Timm 2005).
1.2.2 Biology of false codling moth
1.2.2.1 Eggs
The eggs of FCM measure one millimetre in diameter, are hemispherical in shape, and are translucent. Oviposition on the principal citrus host usually occurs within depressions that are
3
present in the rind of the fruit. The size of the eggs and the selection of oviposition sites render the eggs inconspicuous. The eggs are usually laid one by one, unless female moths have direct access to the flesh of the fruit, usually via a break in the rind; at such locations the eggs may be laid in clusters (Stofberg 1954). The eggs can also be laid in aggregate around the navel of navel oranges (US Department of Agriculture 2010). The eggs can be laid in great quantities; some fruit have been observed with up to 100 eggs (Stofberg 1954). The eggs hatch at all times of the day (Newton 1998).
1.2.2.2 Larvae
The first-instar larvae are vulnerable and can suffer high mortality rates due to low humidity under laboratory conditions and low temperatures, particularly during winter conditions in the field (Newton 1998). Intra-specific competition is a factor in the populations of younger larvae, as the larvae may be cannibalistic when concentrations of larvae are very high, or when food resources are not sufficient (Newton 1998). The delicate first-instar larvae rely on pre-existing cracks or wounds in the rind, or the navel ends of navel oranges, to gain access to the interior of the fruit. Only on rare occasions is more than one larva capable of completing their development within one fruit (Catling & Aschenborn 1974). Stotter (2009) found that acorns could in a similar capacity accommodate more than one FCM larva at a time.
The younger larvae have a creamy white body with a brown-black head capsule (Newton 1998). Mature larvae develop a much more noticeable pink body colour and range between 15 and 20 mm in length. The larval development encompasses five instars. Under field conditions, larval development is completed within the range of 25 to 67 days (Stofberg 1954). The time it takes to complete larval development is dependent on prevailing conditions, with temperature being one of the more dependent factors (Stofberg 1954). Food quality was also found to be an important factor in the development of the larvae. Consistent with observations by Newton (1998) found that fifth-instar larvae which leave the fruit, open conspicuous exit holes and drop to the ground to pupate or emerge when the fruit has already dropped from the tree.
1.2.2.3 Pupae
After exiting the fruit, fifth-instar larvae spin a silk cocoon that binds with soil particles and surrounding detritus (Newton 1998). The finished cocoon, which at this point resembles the soil, lies upon the surface of the soil (Stofberg 1954).
4
Two sub-stages occur within the cocoon: a pre-pupal stage and a pupal stage (Stotter 2009). The pre-pupal stage, which occurs shortly after the spinning of the cocoon, is light beige in colour (Newton 1998). The pupal stage that follows the pre-pupal stage is darker in colour and persists until eclosion occurs (Stofberg 1954). The pupal stage of FCM is completed within 21 to 80 days under field conditions, and the exact duration is dependent on conditions that govern pupal growth, mainly temperature.
1.2.2.4 Adults
Adult FCM are small, inconspicuous moths which tend to be brown-black to grey in colour (Newton 1998). The wingspan is 16 to 20 mm. The anterior wings are mottled and larger and comprise the maximal extent of the wingspan, while the smaller posterior wings are a paler grey colour (Newton 1998).
Male moths are smaller than the females, and are distinguished by densely packed and elongated scales on the hind tibia, an anal tuft of scales, and an olfactory organ near the anal angle of each hind wing (Newton 1998).
Female moths mate within two to three days after eclosion and commence with oviposition as soon as conditions and host availability allow it (Stofberg 1954). Female FCM can produce up to 300 eggs during their lifespan (Stofberg 1939). Temperature has a fundamental impact on the oviposition of FCM, as an average fecundity of 460 eggs per female lifespan is produced at a constant temperature of 25 °C, but only 0.4 eggs per female lifespan at 10 °C (Newton 1998). Oviposition can reach a peak at three to five days of age (Catling & Aschenborn 1974). It has been reported, however, that temperature has a significant effect on the pre-oviposition period of an adult female, varying from one day (at 25 °C) to 22 days (at 10 °C), with 50% of the eggs being laid within six to 23 days after oviposition is initiated (Daiber 1980). The sex ratio of FCM adults has been established at the approximate ratio of 1:2 in favour of the males (Daiber 1980). In wild populations, the sex ratio has been established as closer to 1:1 (Newton 1998).
At a constant temperature and optimal captive conditions, adults can survive for between 13 and 34 days (Newton 1998). Whilst exposed to more fluctuating conditions in the field, adult life expectancy is up to three weeks (Stofberg 1939). As can be expected from an exothermic organism, the total lifespan of FCM decreases as the temperature increases (Stofberg 1954).
5
The adults are exclusively night fliers (Daiber 1978). Oviposition is assumed to take place only at night, as the moths are not known to be active during the day (Stofberg 1954).
1.2.3 Lifecycle of false codling moth
The complete lifecycle of FCM is 45 to 60 days during the summer months (Stofberg 1954). The lifecycle duration increases during the winter months and lasts between 68 and 100 days. When infesting acorns, the lifecycle lasts an average of 121 days, most of which is taken up by the larval stage (84 to 90 days) (Stofberg 1954).
The incubation period for FCM eggs on citrus is six to eight days in summer and nine to 12 days in winter (Newton 1998). Larval development for FCM on citrus during the summer takes 25 to 35 days and 35 to 67 days in the winter. Pupal development takes 21 to 24 days in summer and 29 to 40 days in winter (Stofberg 1954).
The number of generations per year is dependent on prevailing climatic conditions, particularly temperature. Areas that have moderate temperatures (clearly defined summers and winters) will generally have less than six generations per year. Up to six generations can be expected per year in areas that have higher average temperatures (Stofberg 1954).
In hosts other than citrus, and in particular when food quality is poor and host plants produce drier fruit, no more than three generations per year can be expected (Newton 1998). In Southern Africa, FCM are active throughout the year where a constant supply of host fruit is available (Newton 1998).
1.2.4 Hosts of false codling moth
False codling moths are known to have a broad range of hosts, with potential hosts amongst both wild and cultivated plants (Stotter 2009), yet host specificity for FCM remains uncertain. False codling moths are known as an equatorial pest of cotton in Africa (Newton 1998), a pest of citrus in Southern Africa, particularly in the southern areas (Catling & Aschenborn 1974), and as a macadamia nut borer in Malawi (La Croix & Thindwa 1986).
Citrus damage from FCM is particularly acute in navel orange cultivars (De Villiers & Grové 2006). False codling moths also prefer some varieties of mandarin, satsuma, and star ruby grapefruit (Newton 1998). Valencia oranges and grapefruit cultivars other than star ruby are not generally subjected to heavy infestations (Hofmeyr & Pringle 1998). Lemons have been
6
demonstrated to be non-hosts for FCM when subjected to normal harvesting and packing protocols for export (Moore et al. 2015).
The Pest Risk Analysis for Thaumatotibia leucotreta report compiled by the European and Mediterranean Plant Protection Organization (EPPO) identified 19 confirmed hosts of particular interest for the European and Mediterranean regions (EPPO 2013). Sampling in South Africa found that litchis and macadamia nuts also act as hosts for FCM (Timm 2005). Similarly, peaches, nectarines, and plums were investigated, and found to be hosts for FCM (Blomefield 1989). False codling moths were reared successfully under laboratory conditions on wild plum and wild almonds, and proved capable of infesting Port Jackson willow galls (Honiball 2004). In an attempt to find possible alternative hosts of FCM, it was found that the moth could penetrate and inhabit the stems of jade (Kirkman & Moore 2007).
1.2.4.1 Cultivated hosts
The following list is a collection of some better-known cultivated plant hosts of FCM (EPPO 2013). It must be stated that not all of the mentioned hosts are capable of supporting FCM populations as effectively as the principal citrus host, but all can act as possible habitats and must therefore be considered.
Pepper (Capsicum spp.)
Mandarin orange (Citrus reticulata & hybrids)
Orange (Citrus sinensis & hybrids)
Grapefruit (Citrus paradise)
Cotton (Gossypium spp.)
Litchi (Litchi chinensis)
Macadamia (Macadamia spp.)
Mango (Mangifera indica)
Peach (Prunus persica)
Necatrine (Prunus persica var. nucipersica)
Avocado (Persea americana)
Guava (Psidium guajava)
Pomegranate (Punica granatum)
7 Castor bean (Ricinus communis)
Rose (Rosa sp.)
Eggplant (Solanum melongena)
Grape (Vitis vinifera)
Maize (Zea mays)
False codling moth larvae encountered on flowers were successfully reared to adults. From this information Rosa spp. are considered a host of FCM (EPPO 2013).
1.2.4.2 Damage symptoms
False codling moths lay their eggs on the surface of fruit, and when the larvae hatch, they bore into and feed on the rind of the citrus fruit (Newton 1998). In some cases the larvae bore through the rind and penetrate into the core of the fruit (Stotter 2009). This tunnelling by the larvae in many cases leads to the premature drop of the fruit from the trees. Fruit with exposed flesh are more attractive to gravid FCM females than ripe fruit (Newton 1989). Infested fruit may drop from the trees at the beginning of the growing season (usually November) whilst the fruit is still immature and no more than 15 to 20 mm in diameter (Newton 1989). The rind of citrus fruit infested with FCM takes on a brown to yellow colour around the points of larval entry; these damage symptoms act as possible avenues for further arthropod incursions and fungal infections (Stotter 2009). The overall damage to the citrus industry in 2003 that was attributable to FCM was estimated at R100 million (Moore et al. 2004).
The type of damage that FCM inflict on pecan nuts is similar to the damage caused by CM because the method of pecan husk penetration is similar. The first-instar larvae of FCM are capable of accessing the gap in the husk that occurs due to nut development. The researcher observed that nuts which were completely closed were infested by both CM and FCM, and that the nuts were readily identifiable in both cases due to the development of an oily red sheen on the husk of the nut.
1.2.4.3 Economic significance
South Africa is a major agricultural exporter, with agricultural exports totalling just under R38 billion in 2014 (BFAP 2015). Citrus exports experienced a growth of 25% from 2013 to 2014, which was attributed to an increase in export prices, as the volume stayed the same at
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1.74 million tonnes. The net revenue for citrus exports in 2014 was just under R12 billion (BFAP 2015). Iran placed strict phytosanitary standards on all citrus exports from South Africa, which requires much stricter internal control by the producers and cold sterilisation before export (DAFF 2010). Other countries that require cold sterilisation and export control measures for citrus from South Africa are China, the EU countries, Japan, South Korea, Thailand, and the USA (DAFF 2016).
The US Department of Agriculture (2010) reported FCM to be responsible for a loss of up to 30% in macadamia nut production in South Africa and Israel. False codling moths are not known to represent an economic threat to the pecan industry by means of direct damage to crops, but due to the phytosanitary status of the moth, export markets could be in jeopardy if shipments are found to contain FCM.
False codling moths have been found to travel significant distances (1.5 km) to preferred citrus orchards (Stotter 2009). The number of males which shuttled to fynbos, was very low and a significant portion of the FCM population remained in the citrus orchards. False codling moths do not generally shuttle to nearby fynbos vegetation (Stotter 2009); any FCM found within the fynbos were found to be a direct representation of the FCM population in the nearest orchard (Stotter 2009). Guava and acorns were infested within a 1.5 km radius, indicating that nearby potential hosts will initiate FCM shuttling to high densities of such potential hosts (Stotter 2009). Adjacent crops of cotton planted at different times indicated a significant increase of infestation of older cotton situated adjacent to earlier cotton, with up to 60% of the more mature cotton being infested and destroyed by FCM (Reed 1974).
1.2.5 Geographical distribution of false codling moth
False codling moths are endemic and indigenous to the African continent, with a general distribution south of the Sahara Desert, and mostly concentrated in the tropical and sub-tropical regions of the continent (Newton 1998). False codling moth distribution is also evident in Senegal, Côte d’Ivoire, Togo, and Southern Africa. It is also encountered on islands proximate to the continent south of the Sahara in countries such as Madagascar and Mauritius (Newton 1997). The moth is a known pest on citrus in South Africa, Mozambique, Zimbabwe (Stofberg 1954), Swaziland, and Malawi (La Croix & Thindwa 1986). The moth has also been reported in Israel (Wysoki 1986).
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1.2.6 Control measures for false codling moth
International market forces are driving a higher demand for pest-free citrus fruit, with limited pesticide use during production. The drivers behind the increase in demand are mainly economic but also social, political, climatic, demographic, and even emotional. To keep citrus production high and increasing in an area that has endemic populations of FCM, without the egregious use of pesticides, is not necessarily an easy proposition. Existing control methods and newly developed ones, used in conjunction, can enable citrus production to remain significant in South Africa. However, keeping domestic production as well as the quality of the citrus competitive in an ever-changing global market is proving challenging. Ever-stricter phytosanitary and quality restrictions upon producers are placing great strain upon established control methods (Government Gazette 2014). It is therefore imperative to develop new strategies to augment the ability to control FCM or to combine existing strategies in order keep the situation under control.
1.2.6.1 Cultural control
One of the more effective control methods to reduce the population of FCM is the cultural practice of removing fallen fruit from orchards. Visibly damaged fruit should also be removed from trees, as these may not only be infested with larvae, but damaged fruit are also known to be attractive to the moths as oviposition sites (Stotter 2009). Orchard sanitation is a vital pest-control measure and the daily removal of damaged fruit will deliver the best possible results. Out-of-season fruit should also be removed from trees as they may also act as possible hosts for FCM (Moore & Kirkman 2009).
Moore and Kirkman (2009) made the following orchard sanitation recommendations for the control of FCM in citrus orchards:
Remove all out-of-season fruit and unharvested fruit as soon after harvest as possible.
Orchard sanitation must include removal and destruction of dropped fruit and hanging fruit which appear injured, infested, or decaying.
Fruit should ideally be destroyed by pulping or burying (30 cm deep and compacted).
Pulped fruit should be spread on the ground at least 30 m outside orchards.
Fruit 15 mm in diameter and smaller (during November) can be raked into the inter-rows to bake in the sun; however, removal and destruction are still preferable.
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Orchards should ideally be sanitised twice a week during the hotter months of the year (particularly January to March).
1.2.6.2 Biological control
Biological control of FCM forms an important part of the natural pest control in many citrus-producing areas (Stotter 2009). Twenty-five species of natural enemies of FCM have been listed; all potentially occurring in citrus orchards. Of the 25 species, 12 occur in South Africa (Moore 2002). Hymenopteran parasitoids comprise five of the 12 species, two are dipteran parasitoids, another two are insect predators, with two fungal entomopathogens, and finally a baculovirus (Stotter 2009). False codling moth eggs are susceptible to parasitism by trichogrammatid egg parasitoids for the first three to six days of their lifespan (Schwartz 1981). The augmentative release of FCM egg parasitoids in the form of Trichogrammatoidea
cryptophebiae has thus been the focus of commercial biological control attempts (Schwartz
1981). The seasonal increase of FCM is followed by an abundance of T. cryptophebiae (Catling & Aschenborn 1974). Catling and Aschenborn (1974) recommended augmentative mass releases of T. cryptophebiae in the beginning of the citrus season. Schwartz (1981) investigated the augmentative release method and was met with success. It has the potential throughout the season to result in the significant reduction of FCM numbers.
Cryptogran® (River Bioscience (Pty) Ltd, South Africa) is a granulovirus preparation that is applied as a spray formulation to leaf and fruit surfaces. The application of the formulation is regarded as a form of biological control, as the virus is a naturally occurring pathogen of FCM known as Cryptophlebia leucotreta granulovirus (Moore et al. 2004). Emerging larvae, which attempt to bore into the fruit, ingest the virus, and after they die, large amounts of viral bodies are distributed back onto the plant surface, which may potentially infect other FCM larvae. One of the primary advantages of Cryptogran® is that the product can be used in conjunction with a chemical control programme without lowering the overall effectiveness of the virus itself (Stotter 2009). Also, since the virus is specific to the species of its homologous host, it does not have a detrimental impact on FCM’s natural enemies, is harmless to most other insects and vertebrates (including humans), and does not leave residue on the fruit that can be problematic for markets (Moore et al. 2012).
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1.2.6.3 Mating disruption
High-density female sex pheromones of FCM in the form of products such as Isomate (Pacific Biocontrol Corporation, USA) disrupt mating over large areas, if distributed homogeneously (Hofmeyr & Pringle 1998). This has the effect of reducing the number of fertilised eggs that are laid on the citrus fruit. The high dosage of female sex pheromones released at one point has the effect of confusing the males as to the location of the females, thus reducing the overall number of successful mating instances (Carde & Minks 1995). Checkmate FCM-F (Suterra LLC, USA), a spray-applied capsule suspension, does not appear to have the same efficacy as Isomate (Moore & Kirkman 2011). The use of Checkmate FCM-F is nonetheless considered viable for low-pressure FCM regions (Moore & Hattingh 2012).
1.2.6.4 Attract and kill
A product such as Last Call FCM® (Insect Science SA, South Africa) combines synthetic pheromones with a permethrin pyrethroid in one simultaneously deployable product at a density of up to 3 000 droplets per hectare. The product comes in pre-calibrated form to provide consistent 50 μl droplets with a hand applicator. When the female sex pheromone succeeds in drawing the male towards the droplet, contact with the droplet results in the death of the male, which leads to lower rates of fertilisation (Stibick et al. 2007). The product can be effective in the suppression of light FCM infestations, but without the ability to predict the intensity of an infestation, it makes this labour-intensive product difficult to deploy in efforts to curb an infestation (Hofmeyr & Pringle 1998).
1.2.6.5 Sterile insect technique
Only males are considered important for the sterile insect technique (SIT), and to have an effect, an oversaturation of 1:10 in favour of irradiated males is desired in order to ensure effective control (Hofmeyr & Hofmeyr 2004). The eggs produced by the females which mated with treated males will be non-viable in most instances. If any of the eggs do hatch into the new generation (known as the F1 generation), the members of that generation will be sterile. The treatment of the F1 generation is the large-scale irradiation of male and female FCM that are exposed to a 150 Gγ dose of radiation. The irradiated insects are then released into orchards in order to compete with wild insects of the same sex for mates. This culminates in potentially effective FCM control due to the infusion of significant numbers of sterile individuals into the
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population. These populations generally produce fewer viable eggs, and, as a consequence, fewer larvae to damage citrus. It remains more important to uphold the oversaturation ratio with new releases into an area to compensate for the deaths of the treated individuals and their very few offspring.
The implementation and eventual full deployment of F1 SIT seem to be a promising avenue for the control of FCM (Schwartz 1975). In 2002, an SIT project was initiated in the Olifants River Valley (Hofmeyr et al. 2015). Favourable results of pilot studies led to the development and construction of FCM-specific rearing equipment and mass-rearing facilities (Hofmeyr et
al. 2015). By 2010, the project had expanded to apply SIT to 4000 hectares, with a tenfold
reduction in the wild male population (Hofmeyr et al. 2015).
1.2.6.6 Chemical control
Chemical control agents are only economically viable against the egg stages and emerged larvae, with no insecticides registered for use against FCM until the early 1980s. Hofmeyr (1977) demonstrated that synthetic pyrethroids remained effective against FCM for up to 17 weeks. Trials conducted in 1978 and 1983 using cypermethrin and deltamethrin on navel oranges to prevent fruit drop reduced the fruit drop by 90% when applied in one dose, 60 to 90 days before harvest (Hofmeyr 1983).
Trials conducted using the benzoyl-urea chitin synthesis inhibitors, Alsystin® (Triflumuron: Bayer Cropscience, Australia) and Nomolt SC® (Teflubenzurom: BASF Crop Protection, Belgium) indicated that these insecticides had little effect on FCM adults and their larvae (Hofmeyr 1984). Eggs that were laid on spray residue of chitin synthesis inhibitors suffered prolonged suppression. The residues of Alsystin caused up to 85% egg mortality for up to 75 days (Hofmeyr 1984).
The use of Alsystin® and Nomolt SC® as registered FCM products has come under question due to reports of emerging resistance against the effects of the products (Hofmeyr & Pringle 1998). In addition, Alsystin® is known to have detrimental effects on T. cryptophebiae (Hattingh & Tate 1997). Two new chemical insecticides were introduced in 2011 – Coragen (Rynaxapyr: Dow Chemical Company, USA) and Delegate (Spinetoram: Dow Chemical Company, USA) – which were found to have comparable efficacy (Moore & Hattingh 2012). Coragen and Delegate have highly favourable eco-toxicology profiles, making them compatible with IPM strategies and suitable for the widespread establishment of acceptable
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residue tolerances (Moore & Hattingh 2012). In 2013, Runner 240 SC (Methoxyfenozide; Dow Agrosciences SA, South Africa) was introduced as a moult-accelerating compound for the control of FCM on avocados and citrus.
1.3 Ecology of the carob moth
1.3.1 History and taxonomy of the carob moth
The pyralid moth known as Ectomyelois ceratoniae, or carob moth, was redescribed by Philipp Christoph Zeller in 1839. Many synonyms were used over the years, but have since fallen out of use; however, the synonym Apomyelois ceratoniae was in use recently in some parts of the world (Mehrnejad 1993). It is historically known as a pest of wild fruit around the Mediterranean Sea; however, the exact original host remains unclear. Gothilf described the moth as polyphagous in 1964, and as a consequence of the native environment it can be assumed that the moth evolved as a generalist borer of fruits and pods around the Mediterranean Sea. In addition to being adaptable to new hosts within its original range, the carob moth was able to migrate to new habitats and establish itself as a significant pest in areas outside its original distribution (Gothilf 1964). As a demonstration of the essentially cosmopolitan distribution of carob moth, it has been known since the 1960s that carob moth were present on almonds in Australia (Madge 2012). However, it only became an economically significant pest in the early 21st century due to weather changes and expansion into production areas. Carob moth is also the most prominent pest on dates in the state of California in North America (Madge 2012).
1.3.2 Biology of the carob moth
1.3.2.1 Eggs
Carob moth eggs were found to hatch in 3.05 days under laboratory conditions (Mediouni & Dhouibi 2007). Female CM that were kept in mass-rearing conditions produced significantly fewer eggs in comparison to wild females. The difference in egg production was attributed to the lack of space available for copulation (Mediouni & Dhouibi 2007). Mediouni & Dhouibi 2007 observed that when female carob moth were mass-reared, they produced an average of 115.6 eggs per female, of which 95.9 were fertile. Female carob moth reared in single-pair situations produced, on average, 182.5 eggs, of which 140 were fertile. Carob moths are known
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to show preference for oviposition onto already damaged fruit, which increases the survivability of the vulnerable first-instar larvae (Hashemi-Fesharaki et al. 2011).
1.3.2.2 Larvae
Carob moth larvae hatch from the eggs after an average of three days. At temperatures of 28 ± 1 °C, a photoperiod of 14:9 (Light:Dark), and 45 ± 5% relative humidity, the first and most vulnerable larval instar also takes the longest to develop; measured at five days under laboratory conditions (Mediouni & Dhouibi 2007). Under similar conditions it takes the second- and third-instar larvae 4.5 days each to develop, the fourth-instar larvae develop in 4.6 days, and the fifth-instar larvae take 4.8 days to develop to the point where pupation takes place (Mediouni & Dhouibi 2007).
1.3.2.3 Pupae
The CM larvae leave the confines of the host nut or fruit to pupate. The pre-pupating larvae might bore a new tunnel and thus create an extra wound on the surface of the fruit in order to accomplish this, or simply exit via the first tunnel. Pupation may take place in the soil and the larvae spin a cocoon similar to that of FCM, to aggregate substrates into the silk and make the cocoon less visible to potential predators and parasitoids. There are also reports of larvae pupating in the nuts (Mehrnejad 1993). The pupal stage of CM is completed within 6 to 10 days under field conditions, which depends on the conditions that govern pupal growth – mainly temperature (Madge 2012). This was confirmed when a comparison between mass rearing (7.33 days) and single-pair rearing (7.01 days) under laboratory conditions was conducted (Mediouni & Dhouibi 2007). This study observed that larvae will spin a cocoon on the surface of a fruit if no suitable substrate (such as sand) is available for the larvae to utilise. It was also observed that the larvae may make use of the confines of a pecan shell or a pecan husk to spin a cocoon.
1.3.2.4 Adults
Adult CM are inconspicuous moths and have a pale brown pattern on the anterior wings, with plain white posterior wings. Adult CM emerge after a six- to ten-day pupal period, and if conditions are suitable, they will mate and start oviposition immediately (Madge 2012). Under field conditions, the adults have a short lifespan – usually no more than two weeks; however,
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colder temperatures allow the adults to survive longer (Madge 2012). By observing adult lifespans under laboratory conditions, Mediouni and Dhouibi (2007) found that male CM survived on average six days, whilst females survived on average 8.7 days. Under laboratory conditions, female CM are both larger and heavier than the males, with an average adult weight of 24.7 mg; the average male weight was 16.6 mg (Mediouni & Dhouibi 2007).
1.3.3 Lifecycle of the carob moth
Carob moth eggs are usually deposited individually on fruit (Gothilf 1969). The physical condition of the fruit may lead to clusters of eggs being laid in order to take advantage of exposed flesh on the fruit (Hashemi-Fesharaki et al. 2011). Mozaffarian et al. (2007) observed that CM emerge from early May (late spring) in Iran. Pomegranates are attacked first as the conditions on the fruit are deemed most suitable for oviposition (Mozaffarian et al. 2007). The pomegranate (Punica granatum), particularly the sour cultivar, is prone to skin cracking, which increases the prevalence of CM infestation (Hashemi-Fesharaki et al. 2011). Madge (2012) observed that CM in Australia preferred nuts from the previous season still present on the trees as hosts for renewed oviposition. The range of the lifecycle from egg to adult is 34 to 61 days (Reuther et al. 1989). The length of each stage depends on both the climatic conditions as well as the quality of food available for the growth of the larvae. During most years in the USA, four complete generations and a partial fifth generation occur on a yearly basis (Reuther et al. 1989).
1.3.4 Hosts of the carob moth
Some of the better-known hosts of CM have been identified as Ceratonia siliqua, Acacia
farnesiana, Ficus carica, and citrus varieties (Gothilf 1964). The pest is considered
polyphagous as it is capable of attacking both pomegranates and pistachio nuts, which is of considerable concern in Iran (Hashemi-Fesharaki et al. 2011). After completing some generations on pomegranates, as soon as other host plants provide suitable conditions for laying eggs, such as the grooves and tracks that occur on pistachios, CM will infest pistachio nuts as well (Mehrnejad 1993).
Gothilf (1964) found that the presence of fungal infections of Phomopsis spp. on carob pods leads to increased CM oviposition. In addition, gravid CM females, given the opportunity, will prefer to oviposit on nuts infested with Phomopsis spp. (Gothilf 1964). A series of trials
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conducted in Cyprus demonstrated that in order for grapefruit to be infested by CM, an established citrus mealybug (Planococcus citri) infestation was a prerequisite (Serghiou 1983). If no P. citri infestation was present on the surface of the grapefruit, gum exuded by the fruit was able to kill the first-instar CM larvae before they managed to cause significant damage to the fruit (Serghiou 1983).
1.3.4.1 Cultivated hosts
The following list is a collection of the more economically important crop plants which are attacked by the CM.
Almond (Prunus amygdalus)
Carob (Ceratonia siliqua)
Castor oil (Ricinus communis)
Orange (Citrus sinensis)
Date (Phoenix dactylifera)
Fig (Ficus carica)
Grapefruit (Citrus paradisi)
Macadamia (Macadamia integrifolia)
Pecan (Carya illinoinensis)
Pistachio (Pistacia vera)
Pomegranate (P. granatum)
Walnut (Juglans regia)
1.3.4.2 Damage symptoms
The physical condition of the pomegranate neck, which protects the eggs and leads larvae to the inside of the fruit, has an influence on where oviposition takes place (Mozaffarian et al. 2007). Due to this, CM larvae are capable of boring through weak plant tissue that is present in this area and penetrating into the fruit (Mozaffarian et al. 2007). The feeding behaviour of CM presents an opportunity for secondary infestations by fungal and bacterial pathogens (Hashemi-Fesharaki et al. 2011).
The means by which CM penetrate citrus fruit is very similar to the mechanism by which FCM gain access. That is to say, the larvae hatch, bore into, and feed on the rind of the citrus fruit
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(Newton 1998). In some cases, the larvae bore through the rind and penetrate into the core of the fruit (Stotter 2009). The feeding of CM larvae results in premature discolouration of the fruit and to fruit eventually dropping (Reuther et al. 1989). The similar progression of discolouration with the eventual result of fruit drop in citrus indicates that it is a physiological reaction of the plant to the feeding of CM and FCM larvae which results in the symptoms. Thus, many of the damage effects described above concerning the action of FCM on citrus may be similar to the damage that CM inflict on citrus.
The penetration of the nut and the subsequent damage to the nut caused by the feeding action render the nut unsuitable for human consumption (Madge 2012). The penetration of nut crops (as with pomegranates and citrus) generates concern regarding the potential increase in risk for fungal infections (Madge 2012). The first-instar larvae of CM are capable of accessing the gap in the husk that occurs due to nut development. Also, it is assumed that CM are capable of accessing closed nuts by penetrating through the weak point that exists at the base of the stem attachment to the nut. The researcher observed that entirely closed nuts were infested by both CM and FCM (however, never at the same time), and that the nuts were readily identifiable in both cases due to the development of an oily red sheen on the husk of the nut.
1.3.4.3 Economic significance
Carob moths were found to cause significant damage to the fruit of the carob tree in the Mediterranean region (Wood 1963). Wood 1963 noticed in the early 1960s that the CM was starting to establish itself as a citrus pest in the Mediterranean. After investigations during harvest in a carob plantation, Gothilf (1964) found that the magnitude of CM infestation depends on the proportion of cracked fruit in each plantation. Only eggs and young CM larvae were present on grapefruit and this was very seldom (Gothilf 1969). Carob moth eggs are laid individually on citrus fruit and very few were found during the monthly samplings; therefore the damage of CM to grapefruit is considered minimal (Gothilf 1969). The recent expansion of the almond industry, combined with higher-than-average rainfall in Australia, has prompted the rise of CM as a significant pest of an emerging industry (Madge 2012). Similarly, the conditions that led to an increase of CM on almond nuts in Australia now threaten the date (Phoenix dactylifera) industry as well (Madge 2012).
In Iran, CM are considered one of the most important factors responsible for the quantitative and qualitative reduction of pomegranate yield throughout the pomegranate cultivation regions
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of the country. Carob moths also attack pistachio orchards in Iran (Hashemi-Fesharaki et al. 2011). Appropriate weather conditions and the suitable physical properties of the fruit (early maturity and sensitivity to skin cracking) are considered the two main reasons for an increase in infestation (Hashemi-Fesharaki et al. 2011). In most cases where secondary infestations are not significant, loss of fruit quality due to moisture loss and feeding damage lowers the marketability of the produce (Hashemi-Fesharaki et al. 2011). Shakeri (2004) found that within the primary pomegranate production areas of Iran, CM could infest and thus render up to 80% of the crop unmarketable during the fruiting season and at harvest. Carob moth infestations have been found to be notably high in pistachio orchards adjacent to pomegranate plantations. It was found that CM attack pistachio nuts during the early summer, hence the requirement for an alternative host in the spring. In the absence of an alternative host, CM are not able to establish in pistachio orchards (Mehrnejad 1993; 1995).
1.3.5 Geographical distribution of the carob moth
While CM are a well-known pest in the Mediterranean, they are also present in other parts of the world, including Hawaii, the USA, as well as the tropical and subtropical regions of the Americas (Gothilf 1969). Heinrich (1956) postulated that CM were introduced to the New World directly from the Mediterranean. In the Americas they are widely distributed throughout the USA and are present in Argentina and the West Indies (Reuther et al. 1989). Carob moths also occur in Australia, where they cause significant damage to the almond industry.
1.3.6 Control measures of carob moth
1.3.6.1 Cultural control
Gothilf (1964) observed that CM develop mostly in cracked carob pods. Of the pods investigated at harvest, 70% to 90% of all cracked pods were found to be infested by CM (Gothilf 1964). The removal of carob pods from the previous season was strongly encouraged, as infestation of the pods increases as the season progresses (Gothilf 1969).
For the control of CM in almonds, the removal of almonds still present from the previous season proved to be effective to reduce the pest population (Madge 2012). The previous seasons’ nuts were found to be preferred habitats, which housed up to six CM larvae per nut; in contrast to nuts from the current season, which only harboured an average of two. The manual removal of nuts from the previous season was strongly encouraged (Madge 2012).
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Al-Izzi et al. (1985) reported that orchards in Iran that demonstrated poor sanitation procedures had the highest incidence of CM. Sanitation procedures such as the removal and destruction of dropped pomegranate fruit are encouraged in order to remove potential additional hosts for future populations of CM to reproduce (Al-Izzi et al. 1985).
Infected pomegranates might not be the only overwintering sites for CM (Mozaffarian et al. 2007). This suggests that the removal of pomegranates left after harvest may only reduce, rather than prevent the overwintering of CM (Mozaffarian et al. 2007). The same study found that high levels of CM infestation on host plants other than pomegranates were not present. Mozaffarian et al. (2007) suggested that cultural control practices should not only focus on the sanitation of pomegranates but also on other potential overwintering hosts could become significant factors in the future, such as pistachio nuts.
1.3.6.2 Biological control
In 1946, only one species of braconid wasp, Habrobracon brevicornis, was recognised as a natural enemy of the CM (Thompson 1946).
In Israel it was found that CM were parasitised in carob tree plantations. The parasitism was mainly attributed to the braconid Phanerotoma flavitestacea and the tachinid Clausicella
suturata (Gothilf 1969). Carob moth infestation of carob pods can reach a maximum of 56%
in carob plantations (Gothilf 1969). Similarly, the incidence of parasitised insects seemed to be linked more to the location of the carob plantation rather than to the carob variety, and seemed to vary from year to year. Gothilf (1969) also observed that parasitism of CM increased as the carob season ended, with the incidence of parasitism averaging 20% to 50% during August. The incidence of CM egg parasitism was found to be low, with only isolated instances of parasitism by Trichogramma spp. being recorded (Gothilf 1969).
When infesting carob plantations, only small numbers of parasitoids of CM other than P.
flavitestacea and C. suturata were collected (Gothilf 1969). The other parasitoids noted were
as follows: Baronia brevicornis, Apanteles lacteus, Apanteles spp., Anisopteromalus mollis,
Pristomerus vulnerator, Horogenes spp., Gelis spp., Brachymeris aegyptiaca (possibly a
hyperparasite), Antocephalus mitys, and Perilampus tristis (Gothilf 1969). Other species also collected were a number of hyperparasites such as Gelis spp., B. aegyptiaca, and P. tristis, with
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Many of the abovementioned species were recorded for the first time as parasitoids of CM on carob, in particular members of the genus Apanteles in 2012 (Kishani Farahani et al. 2012). A recent study found that female Apanteles myeloenta typically preferred to parasitise second-instar CM over third- or first-second-instar CM (Kishani-Farahani et al. 2012). The oviposition activity of A. myeloenta on the CM larvae peaks on the seventh and eighth days following the emergence of the adult parasitoids from pupae (Kishani-Farahani et al. 2012). Parasitism of CM by A. myeloenta was noted to be particularly high, with up to 30% of larvae and up to 25% of the overwintering larvae being parasitised during cultivation (Kishani-Farahani et al. 2012). Kishani-Farahani et al. (2012) found that the sex ratio of A. myeloenta was of profound importance for the parasitoid to act as a potential biological control agent. The larval stages parasitised was found to have the greatest influence on the sex ratio, therefore second-instar CM larvae were the best option to maximise the overall number of female A. myeloenta that emerged (Kishani-Farahani et al. 2012). The availability of carbohydrates for adult feeding of
A. myeloenta was also found to increase longevity and fecundity, both of which are important
for the agent to act as efficiently as possible for as long as possible (Kishani-Farahani et al. 2012).
1.3.6.3 Mating disruption
Various forms of pheromone dispensers for the disruption of CM mating have been developed. The function of the dispenser is to confuse male CM as to the location of potential females (Carob Moth UC IPM Fact Sheet, UC Davis College of Agricultural & Environmental Sciences 2012). The half-life and pheromone release rate of traps vary to a great degree; female sex pheromones are utilised in this capacity. The chemicals used by each company are usually proprietary in nature and results between traps tend to vary accordingly. There have also been suggestions that large-scale deployment of a selected pheromone solely for the purpose of mating disruption could be a viable option. This can be done by dispersing large quantities of sex pheromone within an area to confuse the male CM (Madge 2012).
The oil extracts of Asant (Ferula asafoetida) have shown to be efficient in repelling CM (Peyrovi et al. 2011). The application of a 4 ml solution of F. asafoetida oil and ethanol (in a 50/50 proportion) onto a section of fabric, inserted into a polycarbonate tube, 20 tubes per hectare, achieved the best results (Peyrovi et al. 2011). To ensure optimal potency, the solution
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should be reapplied on a monthly basis. A suspension of the Asant solution was also shown to be a potential oviposition disruptor for CM (Peyrovi et al. 2011).
1.3.6.5 Sterile insect technique
The development of an SIT programme for CM was last reported to be in the pilot phase (Simmons et al. 2009). Only limited releases of CM took place, with efforts still focused on formulating an artificial diet that could increase the fertility and fecundity of adult CM (Mediouni & Dhouibi 2007). It is essential that irradiated males are capable of competing with wild males (Mediouni & Dhouibi 2007). Irradiated males were found to be able to compete with wild males after limited releases and sex pheromone trap captures indicated statistically insignificant discrepancies between wild and irradiated males recovered from the traps. It was concluded that irradiated CM males still respond to virgin female pheromone dispersal. Mediouni and Dhouibi (2007) stressed that more research needed to be conducted regarding the formulation of the artificial diet. Mediouni and Dhouibi (2007) also indicated during the progression of their study that CM were highly resistant to radiation, requiring more than 400 Gγ in order to ensure complete sterility in the females but only partial sterility in the males.
1.3.6.6 Chemical control
The developmental biology and behaviour of CM larvae are not amenable to the widespread use of chemical insecticides for control (Kishani Farahani et al. 2012).
An effective measure of chemical control over CM was achieved with the application of Trichlorfon (Organophosphate: Miles, Inc., USA) or fenthion (Organophosphate: Bayer CropScience, South Africa) over a period of 10 days (Reuther et al. 1989). Mecarbam (Methylcarbamate: Sigma-Aldrich, USA), originally formulated as a scalicide, was tested in Cyprus as an effective means of control for CM (Serghiou 1983). The combined application of chlorpyriphos (Organophosphate: DowElanco, USA), mecarbam, methomyl (Carbamate: DuPont Agricultural Products, USA), and methidathion (Organophosphate: Ciba-Geigy Corporation, USA) were effective in controlling both citrus mealybug and CM infestation when they occured together as a complex (Serghiou 1983).
It has been suggested that the use of products such as Naturalyte® (Spinosad: Dow AgroSciences LLC; USA) is the best option for the control of CM within an IPM programme (Carob Moth UC IPM Fact Sheet 2012). As an insect growth inhibitor, Fenoxycarb
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(Carbamate: Syngenta Crop Protection (Pty) Ltd, South Africa) has been suggested for use within an IPM programme (Carob Moth UC IPM Fact Sheet 2012). It is recommended that insecticides should be applied within a week of the first trap captures of CM in order to ensure the maximum chance of treating the exposed first-instar larvae before they move into the crop (Carob Moth UC IPM Fact Sheet 2012).
1.4 Ecology of the grey-brown stink bug
1.4.1 History and taxonomy of the grey-brown stink bug
Dallas described the grey-brown stink bug as Coenomorpha nervosa in 1851. As a member of the family Pentatomidae (Hemiptera), the grey-brown stink bug shares many biological traits with other Pentatomidae, specifically with species that indicate a convergence of preferences for inhabiting similar environments and damaging the same plants. Coenomorpha nervosa is a pest of avocado. Other Pentatomidae are also known pests, such as the green stink bug (Nezara
viridula) and the powdery stink bug (Atelocera raptoria) (Bruwer 2004). The aforementioned
species are not necessarily closely related but share similar preferences for host plants. This convergence makes it convenient and in some cases necessary to substitute the habits and preferences of the better-studied species (A. raptoria and N. viridula) with the tendencies of C.
nervosa. This is sometimes necessary due to the lack of available literature that refers directly
to C. nervosa.
Coenomorpha nervosa has not distinguished itself as a key pest and any development of control
measures occurs with methods for A. raptoria, N. viridula, and other hemipteran species (Bruwer 2004). This indicates that C. nervosa is considered very similar to A. raptoria and N.
viridula from a pest control viewpoint and as such can be treated as having similar biologies
(Bruwer 2004).
1.4.2 Biology of the grey-brown stink bug
1.4.2.1 Eggs
Coenomorpha nervosa eggs are laid in clusters, and are very similar in appearance and in the
number of eggs laid to that of the brown marmorated stink bug, Halyomorpha halys (Bernon
et al. 2004). The egg clusters usually number around 25 eggs, of which each is about 1 mm in
